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Functional defecation disorders in children
Associated comorbidity and advances in management Kuizenga-Wessel, S. Publication date 2017 Document Version Other version License Other Link to publicationCitation for published version (APA):
Kuizenga-Wessel, S. (2017). Functional defecation disorders in children: Associated comorbidity and advances in management.
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Chapt%r t"$
ADHD AND FUNCTIONAL
DEFECATION DISORDERS
IN CHILDREN
S. Kuizenga-Wessel, I.J.N. Koppen, M.H. Vriesman, C. Di Lorenzo,
M. van Dijk, M.L.R. Beelen, M. Groeneweg, R.J. Stoffelsen, M.A. Benninga
ABSTRACT
Objectives
To assess the prevalence of attention deficit hyperactivity disorders (ADHD) in children presenting with functional defecation disorders (FDDs) and to assess the prevalence of FDDs in children with ADHD.
Methods
A cross-sectional cohort study was carried out between September 2014 and May 2016, in which two groups of patients were included. Group 1: Parents of chil-dren with FDDs according to the Rome III criteria completed the Child Behavior Checklist (CBCL) and the VvGK (Dutch questionnaire based on the American Disruptive Behavior Disorder rating scale). Patients with ADHD subarea scores ≥70 on the CBCL and/or ≥16 on the VvGK were referred for further psychiatric evaluation. Group 2: Parents of children treated for ADHD at a specialized ADHD-outpatient clinic completed a standardized questionnaire regarding their child’s defecation pattern.
Results
In group 1, 282 children were included and concomitant ADHD was diagnosed in 10.3 (7.1 – 13.5% BCaCI). Group 2 consisted of 198 children and 22.7% (17.6-28.8 BCaCI) fulfilled the Rome III criteria for a FDD. Children with both a FDD and ADHD reported urinary incontinence significantly more often compared to chil-dren with a FDD or ADHD alone: 57.1% in FDD+ADHD vs. 22.8% in FDD alone (p<0.001) and 31.1% in ADHD+FDD vs. 7.8% in ADHD alone (p<0.001).
Conclusion
10.3% of children with FDDs had ADHD and 22.7% of children with a known diagnosis of ADHD fulfilled the Rome criteria for a FDD. This observation suggests that screening for behavioral disorders and FDDs should be incorpo-rated into the diagnostic workup of these groups of children.
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INTRODUCTION
Functional defecation disorders (FDDs) are common in childhood and comprise of functional constipation (FC) and functional non-retentive fecal incontinence (FNRFI)1. The estimated worldwide prevalence of FC in children ranges from 0.7
to 29.6%2, while FNRFI is estimated to occur in less than 1% of children in the
general population3. In children with FC, fecal impaction may lead to
over-flow fecal incontinence, while in children with FNRFI fecal incontinence occurs without signs of fecal retention.
Behavioral problems are frequently reported in children with FDDs4–6. Likewise,
gastrointestinal problems like abdominal pain and constipation, are common in children with behavioral disorders, such as attention deficit hyperactivity disorder (ADHD) and autism spectrum disorders (ASD)7–9. ADHD is defined as
a persistent pattern of inattention, hyperactivity and/or impulsivity that causes impairment, with an onset before the age of 7 years10. The estimated
preva-lence of ADHD among school-aged children and adolescents is 5%10,11and this
condition is more common in boys and gender ratios range from 1:3 to 1:1612.
The etiology is multifactorial and largely unknown, but genetic factors, environ-mental and social factors are thought to play a role13.
Reliable data on the prevalence of ADHD in children presenting with FDDs are scant. In a retrospective cohort study using a database of the military health system in the US, children with ADHD had an increased prevalence rate of FC (4.1% vs. 1.5%) and fecal incontinence (FI) (0.9% vs. 0.15%) compared with children without ADHD8. More reliable prospective studies on the prevalence of ADHD
in children presenting with FDDs and vice versa are needed to further clarify the possible association between these two disorders. Novel insights could contribute to optimizing diagnostic and therapeutic strategies in these children. The aim of this study was to prospectively assess 1) the prevalence of ADHD in children presenting with FDDs, and 2) the prevalence of FDDs in children with a known diagnosis of ADHD.
METHODS
A cross-sectional cohort study was carried out between September 2014 and May 2016 in two groups of patients.
GROUP 1 CHILDREN WITH FDD
Children (6-16 years), who met the Rome III criteria for FC or FNRFI and who were treated at the specialized outpatient clinic of a tertiary center and a secondary hospital, were eligible for enrollment1,14. Patients were included
regardless of previous treatments for FDDs or previously diagnosed behavioral health problems. Patients were excluded if they had an organic cause for their defecation disorder. After informed consent was obtained, parents or care-givers were asked to complete two ADHD-screening questionnaires; patients were only included if both questionnaires were returned.
ADHD screening questionnaires
1) The Child Behavior Checklist (CBCL/4-18)15 is a validated parent-report
ques-tionnaire to evaluate various behavioral and emotional problems. We used a validated Dutch translation of the CBCL16. The CBCL assesses internalizing
(i.e., anxious, depressive, and over-controlled) and externalizing (i.e., aggres-sive, hyperactive, noncompliant, and under-controlled) behaviors. It measures several subareas, including attention problems. Questions are answered on a 3-point Likert scale (0= not true, 1=somewhat or sometimes true, 2= very true or often true). Total raw scores are transformed into age- and gender-normed T-scores.
For this study, we only referred children for further behavioral evaluation based on the CBCL if they had clinical scores in the subarea “attention problems”. For this subarea, we used a T-score of ≥70 (98th percentile) as
clinical scores, and T-scores between 65-69 as subclinical scores (93-97th
percentile)15. Furthermore, the “Total CBCL T-score”, as well as the total
scores for internalizing and externalizing problems were calculated (clinical score: ≥64, subclinical score: 60-63).
2) The VvGK17 is a validated Dutch questionnaire based on the ‘American
Disruptive Behavior Disorder rating scale’. The VvGK assesses external-izing behavior and screens for symptoms of ADHD, oppositional defiant disorder (ODD) and conduct disorder (CD). The questions are divided into four subscales: attention-deficit, hyperactivity/impulsiveness, ODD and CD. Parental responses are recorded on a 4-point Likert scale (0= not at all, 1=
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a little, 2=quite a lot, 3=very much). Total raw scores are transformed into age- and gender-normed T-scores. A T-score on the attention-deficit and/ or hyperactivity/impulsiveness-subscales of ≥16 (98th percentile) was used to
identify children with behavioral problems, with a T-score of 15 as subclinical score (95th percentile)17.
GROUP 2 CHILDREN WITH ADHD
Parents of children (6-16 years) with a known clinical based diagnosis of ADHD (according to the DSM-IV classification) treated at a specialized ADHD-outpa-tient clinic, received a letter by mail. This letter contained information about the study, an informed consent form and a questionnaire regarding the child’s bowel habits. We used a standardized defecation questionnaire, developed by the specialized pediatric gastroenterology outpatient clinic of our tertiary center and consisted of questions about medical history, bowel habits, urinary problems and (previous) laxative usage. The questionnaire addresses all Rome III criteria for FC and FNRFI1. Parents were asked to complete the questionnaire
and return it anonymously by mail.
Positive testing policy
GROUP 1 FDD-GROUP
Children with clinical scores exceeding the pre-established cut off values for the CBCL and/or VvGK were referred to a specialized ADHD outpatient clinic for a comprehensive psychiatric diagnostic assessment, this to evaluate whether they met the DSM-IV criteria for ADHD or other behavioral disorders.
GROUP 2 ADHD-GROUP
Parents were given the opportunity to contact one of the investigators (SKW) with any questions regarding the completed defecation questionnaire. If neces-sary, parents were referred to their general health practitioner or seen at the specialized outpatient gastroenterology clinic. Due to the anonymous nature of the questionnaires, children fulfilling the Rome III criteria were not actively approached for an evaluation at the gastroenterology clinic.
Outcomes
The primary outcomes were 1) the prevalence of ADHD in children with FDDs, according to the DSM-IV criteria based on a clinical evaluation and 2) the prevalence of FDDs in children with ADHD, according to the Rome III criteria, based on the questionnaire.
Statistical analyses
For all statistical analyses SPSS version 23 (IBM, Amsterdam, The Netherlands) was used. A maximum of 10 percent missing values was considered acceptable. Parametric data were compared using independent t-tests. For the compar-ison of non-parametric data, Mann-Whitney U tests were performed. For the comparison of proportions, Chi square analyses were performed. Fisher exact tests were performed to compare proportions with an observed or expected frequency of less than 5. P <.05 was considered statistically significant. Bias-cor-rected and accelerated bootstrapping, drawing 100 samples of the same size as the original sample with replacement, was performed to generate 95% bias-corrected and accelerate confidence intervals (BCaCI).
Ethical considerations
The medical ethics committee of the Academic Medical Center of Amsterdam approved the study protocol. All parents gave written informed consent.
RESULTS
FDD-GROUP
Demographics
The baseline characteristics of the 282 included FDD patients are shown in Table 1. Twenty-four patients (8.5%) had been diagnosed with ADHD previous to this study, all of them received treatment; 17/24 used psychopharmacolog-ical medication for ADHD.
ADHD screening questionnaires
The outcomes of the CBCL and VvGK questionnaires are summarized in Table 2. A total of 32 patients (11.3%) scored in the clinical range of either the CBCL or the VvGK or both; 17 patients (6.0%) on the CBCL and 25 patients (8.9%) on the VvGK; with 10 children (3.5%) scored in the clinical range on both questionnaires. Of the 24 patients with a prior DSM-IV diagnosis of ADHD, 11 patients had clin-ical scores on one or both screening questionnaires. Of the remaining 13 chil-dren diagnosed with ADHD, 5 patients had subclinical scores and 8 patients had normal scores on both questionnaires.
Psychiatric evaluation
Out of the 32 patients with positive ADHD-screening questionnaires, 25 parents waived the referral for a comprehensive psychiatric evaluation: 5 parents
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argued that their children were not experiencing problems in daily life and 20 children were currently receiving (non)pharmacological treatment for their behavioral problems elsewhere. Ten out of these 20 children had a diagnosis of ADHD (Table 2); with 4 children having a concomitant DSM-IV diagnosis (ASD or Tic disorder). DSM-IV diagnoses in the remaining patients included ASD (n=4), anxiety disorder (n=3), developmental coordination disorder (n=1). Thus, 7 patients were referred for a psychiatric evaluation. One patient had previously been diagnosed with ADHD, and this diagnosis was confirmed. Five out of seven patients were diagnosed with ADHD, according to the DSM-IV. One was diagnosed with Asperger’s.
As ADHD was previously known in 24 patients and 5 new ADHD diagnoses were made after psychiatric evaluation, the total number of patients with a diagnosis of ADHD in the FDD-group was 29, resulting in a prevalence of 10.3% (7.1 – 13.5% BCaCI).
Table 1 Demographics of FDD group
n= 282
Male, n (%) 171 (60.6)
Age in years, median (IQR) 9.5 (7.3-11.8)
Center of recruitment, n (%)
Emma Children’s hospital/AMC, Amsterdam Maasstad, Rotterdam 270 (95.7) 12 (4.3) FDD diagnosis, n (%) Diagnosis FC without FI Diagnosis FC with FI Diagnosis FNRFI 175 (62.1) 82 (29.1) 25 (8.9) Duration of symptoms in months, median (IQR) 60.0 (36.0-84.0) Treated by general practitioner only, n (%) 120 (35.8) Behavior problems, n (%)
Known diagnosis of ADHD
Known DSM-diagnosis other than ADHD
24 (8.5) 48 (17.0)1
Use of psychopharmacologic medication for ADHD, n (%) 17 (6.0)
ADHD = attentive deficit/hyperactivity disorder, FC= functional constipation, FI = fecal incontinence, FNRFI = functional nonretentive fecal incontinence, IQR=interquartile range 1 Autism spectrum
disor-ders=25; anxiety disorder, n=10; PTSS, n=3; Tic disorder, n=4; eating disorder, n=2; pica, n=1; dysthymic disorder, n=1.
Table 2 ADHD-screening questionnaires and behavior health evaluation
ADHD screening questionnaires
CBCL n=282
Median attentional subarea score, median (IQR) 53.00 (51.0-59.0) Attentional subarea clinical range (T-score ≥70), n (%) 17 (6.0)
Attentional subarea subclinical range (T-score 65-69), n (%) 23 (8.2) Total positive scores, (T-score ≥64), n (%) 86 (30.5) Internalizing behavior problems, (T-score ≥64), n (%) 121 (43) Externalizing behavior problems, (T-score ≥64), n (%) 46 (16.3) VvGK n=282
Median VvGK-A score, median (IQR) 11.0 (10.0-13.0) VvGK-A clinical range (score ≥16), n (%) 24 (8.5) Median VvGK-HI score, median (IQR) 10.0 (10.0-12.0) VvGK-HI clinical range (score ≥16), n (%) 11 (3.9) VvGK-A or VvGK-HI clinical range (score ≥16), n (%) 25 (8.9) VvGK-A or VvGK-HI subclinical range (score =15), n (%) 17 (6.3) Patients with clinical scores n=32
Cases with scores in clinical range on CBCL or VvGK, n (%) 32 (11.3) Cases with both scores in clinical range of CBCL and VvGK, n (%) 10 (3.5) Psychiatric evaluation n=32
Parents approached for a referral, n (%) Previously known DSM-diagnosis, n (%) Waived referral, n (%)
Completed psychiatric evaluations
32 (11.3) 18 (54.5) a,b
25 (78.1) b
7 (21.8) b
DSM-diagnosis based on psychiatric evaluation n=7 ADHD, n (%)
Attention deficit disorder – NOS, n (%) Asperger’s, n (%)
6 (18.8) b, c
1 (3.1) b
1 (3.1) b
ADHD= attentive deficit/hyperactivity disorder, CBCL= Child Behavior Checklist, IQR=interquartile range, NOS= not otherwise specified, VvGK-A= attention deficit subscale on VvGK, VvGK-HI= hyper-activity/impulsiveness subscale on VvGK
a ADHD, n=7; ADHD+Autism spectrum disorder, n=3; ADHD+Tic disorder, n=1; autism spectrum disorder
n=4; anxiety disorder, n=3; and developmental coordination disorder, n=1. b n (% of the parents
approached for a referral for psychiatric evaluation), c 5/6 new diagnosis of ADHD, and 1/6
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Table 3 Clinical characteristics of patients in the FDD group with and without
ADHD according to the DSM-IV criteria
FDD FDD + ADHD p-value
N 254 28
Male, n (%) 154 (60.1) 17 (60.7) 0.99 a
Age in years, median (IQR) 9.3 (7.3 – 11.4) 10.9 (8.3 – 12.5) 0.09 b
FDD subtypes, n (%) Diagnosis of FC without FI Diagnosis of FC with FI Diagnosis of FNRFI 76 (29.9) 156 (61.4) 22 (8.7) 6 (21.4) 19 (67.9) 3 (10.7) 0.24 a 0.33 a 0.46 a
Duration of symptoms in months, median (IQR) 60 (36 – 84) 72 (36 – 96) 0.28 b
Psychiatric comorbidity other than ADHD, n (%) 39 (15.4) 9 (32.1) 0.03 a *
Urinary incontinence, n (%) Nighttime Daytime 51 (20.1) 58 (22.8) 9 (32.1) 16 (57.1) 0.12 a <0.001 a *
ADHD = attentive deficit/hyperactivity disorder, FC= functional constipation, FDD= functional defeca-tion disorder, FI = fecal incontinence, FNRFI = funcdefeca-tional nonretentive fecal incontinence, IQR=inter-quartile range. a Fisher’s exact test, b Mann-Witney U test, *statistically significant
Clinical characteristics of patients with and without ADHD symptoms
Table 3 shows the clinical characteristics of children in the FDD-group, comparing patients with and without a diagnosis of ADHD. Patients with FDD+ADHD reported daytime urinary incontinence (UI) significantly more often compared to children with FDD alone (57.1% vs 22.8%, p < 0.001).
ADHD GROUP
Demographics
Baseline characteristics of the 198 included ADHD patients are shown in Table 4. The majority (n=153, 77.3%) of patients with ADHD used psychopharmacological medication; 23 patients (11.6%) had ≥1 other concomitant psychiatric disorders. The prevalence of FDDs in the ADHD-group was 22.7 (17.6-28.8 BCaCI); 42 patients met criteria for FC and 3 patients met criteria for FNRFI. Six out of 45 children (13.3%) had previously been diagnosed with a FDD and 5 of these patients still used laxatives at the moment of enrollment in this study.
Clinical characteristics of patients with and without FDD symptoms
Clinical characteristics of patients in the ADHD-group were compared between those with and without FDDs (Table 5). Abdominal pain (60.0% vs 30.1%, p< 0.001) and UI (31.1% vs 7.8%, p < 0.001) were reported significantly more often in children with ADHD+FDD compared to children with ADHD alone.
Table 4 Demographics ADHD group
n=198
Male, n (%) 144 (72.7)
Age in years, median (IQR) 11.6 (9.8 – 13.7)
Center of recruitment, n (%) De Bascule, Amsterdam Maasstad Hospital, Rotterdam
118 (59.6) 80 (40.4) Previously diagnosed with FDD, n (%) 6 (3.0) Patients with other psychiatric comorbidity, n (%) 23 (11.6)1
Using psychopharmacologic medication, n (%) 153 (77.3) Meet criteria for FDD, n (%)
Total FC without FI FC with FI FNRFI 45 (22.7) 29 (64.4) 13 (28.8) 3 (6.7)
FC= functional constipation, FDD= functional defecation disorder, FI = fecal incontinence, FNRFI = functional nonretentive fecal incontinence, IQR=interquartile range
1 Psychiatric comorbidity in patients from the ADHD-group: Autism spectrum disorder, n=10; ODD,
n=4; anxiety disorder, n=4; dysthymic disorder, n=3, trichotillomia, n=1
DISCUSSION
This is the first study to prospectively assess the prevalence of ADHD (based on the DSM-IV criteria) in children with functional defecation disorders (FDDs) (based on the internationally accepted Rome III criteria), and vice versa. In our study, 10.3% children presenting with FDDs had a confirmed diagnosis of ADHD and 22.7% of children with a known diagnosis of ADHD fulfilled the Rome III criteria for a FDD. Children with FDDs+ADHD and ADHD+FDDs reported urinary incontinence (UI) significantly more often compared to children with ADHD and FDDs alone.
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The prevalence of concomitant ADHD in children with FDDs (10.3%) found in our sample is higher than the reported prevalence of 5% in the general popu-lation18. Our results corroborate previous studies showing a higher prevalence
of ADHD in children with FDD. In a study by Niemczyk et al., 1,676 parents of German schoolchildren completed a questionnaire regarding FI, UI and ADHD symptoms. ADHD was diagnosed based on DSM-IV items and incontinence was defined based on occurrence of at least once per month. They reported a prevalence of 10.3% of ADHD in children with FI19. These results were
corrob-orated by another population-based study, in which parents of 8,242 children aged 7-8 years, completed questionnaires regarding FI and common behav-ioral problems. In this study, 9.2% of children with frequent FI had ADHD20. The
limitation of these studies was that ADHD diagnoses were based on question-naire-scores, and not confirmed by clinical evaluation. Recently, our group showed that positive ASD-screening questionnaires did not always correctly identify children with ASD21. After psychiatric evaluation, the majority of children
with positive screening questionnaires were diagnosed with other DSM-IV diag-noses than ASD. Together with the results from our current study, this empha-sizes the need for referral in case of positive screening questionnaires.
We found that the prevalence of coexistent FDDs in children with ADHD was 22.7% (FC 64.4%, FC+FI 28.8%), which is higher than the median prevalence of FC reported in a systematic review (12%)2 and higher than the prevalence of FDDs
in children with ADHD reported by McKeown et al (FC 4.1% and FI 0.9%)8. In the
latter study, ICD-codes were used to identify children with ADHD, FC and FI in a military health system database. However, this study did not involve a clin-ical evaluation and it is unclear if standardized criteria, like the Rome III and DSM-IV criteria, were used to diagnose these disorders. Differences between our findings and those from other studies may rely on methodological factors, especially differences in definitions.
Although multiple studies have described an association between FC, FI and ADHD, the pathophysiology of these disorders has not been clarified yet. FDDs and ADHD are heterogeneous disorders in which genetic factors are thought to play a role13,22. Another factor could be an altered communication between
the central nervous system (CNS) and the enteric nervous system, resulting in disturbed gastrointestinal motility8. Others hypothesized that ADHD leads to
FDDs, as children with ADHD ignore their urge to defecate or experience diffi-culties taking the time to complete bowel movements19. Children with ADHD
are also less compliant to incontinence treatment23 and this could also causes
Urinary incontinence has been described to be associated with both ADHD and FDDs20,24,25 and psychological problems have been shown to be
asso-ciated with both UI and FI26. Approximately one third of children with FDDs
has coexistent daytime and nighttime UI27,28. Moreover, successful treatment of
constipation resulted in resolution of UI28. In children with ADHD, nighttime UI
is one of the most common reported comorbidities29,30. Clinical studies have
consistently shown that children with ADHD have high rates of nighttime UI, but much less data is available on daytime UI. In a small study, children with ADHD (n=28) had significantly more nighttime and daytime UI than controls (n=22)31.
In our study, children with FDD+ADHD and ADHD+FDD also reported symp-toms of UI. The connection between these disorders and UI is unknown, but some hypothesize that FDDs and UI are related to maturational disorders of the CNS, resulting in difficulties with responding to urge5. Other possible factors
include fecal impaction leading to bladder obstruction and detrusor hyperac-tivity, or abnormal pelvic floor function32. It is hypothesized that patients with
ADHD frequently have coexisting UI because they share CNS-abnormalities33–35,
but the incontinence may also be due to ADHD-associated inattentiveness33.
The major strengths of our study are the prospective design, the large patient samples and that diagnoses of FDDs and ADHD were made according to the internationally accepted criteria; the Rome III and the DSM-IV criteria. Neverthe-less, there are limitations that should be taken into account when interpreting our results. Firstly, our study is at risk of selection bias towards more severe cases of FDD and ADHD as most of the patients were recruited from tertiary referral centers and patients/parents may have been more willing to participate if they believed that their child may have been suffering from these disorders. This could have resulted in a higher overall prevalence of ADHD in children with FDD, or FDD in children with ADHD. Secondly, it is possible that children with positive screening-questionnaires, who waived their referral for behavior health evalua-tion, have ADHD or meet criteria for another DSM-diagnosis. This could have resulted in an underestimation of the prevalence of ADHD in children with FDDs. The same goes for children who had a clinical total CBCL-score, these children may have been referred for evaluation outside the study, for clinical reasons. The outcome of these referrals was not available to our research team. Lastly, patients in the ADHD-group were not subjected to a physical and rectal exam-ination, which are necessary to determine the presence of a large fecal mass in the rectum, one of the Rome III criteria. It is therefore possible that we have underestimated the prevalence of FDDs in children with ADHD.
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Our findings may have several implications for clinical practice as well as research concerning childhood FDDs. Although the majority of children with behavior problems in the current study were already diagnosed, the use of screening-questionnaires resulted in 6 new DSM-diagnoses. Moreover, 11/24 children that were diagnosed with and received treatment for ADHD still had clinical scores on the ADHD-screening questionnaires at time of the survey. In addition, we identified children with symptoms of internalizing (43%) and exter-nalizing (16.3%) disorders. Since unrecognized behavior problems may inter-fere with the treatment of FDDs, children with FDDs should be screened for behavior problems (like ADHD) routinely. If behavior problems or FDDs are present, referral for and treatment of both disorders is recommended. Espe-cially since treatment outcomes are less successful in children with ADHD36.
Niemczyk et al., showed that treatment of ADHD had positive effects on the prevalence of incontinence23, and van Dijk et al showed that CBCL-scores
decreased after a combination of conventional treatment and behavioral therapy37. Vice versa, healthcare providers should be aware of the high
prev-alence of FDDs and UI in children with ADHD and these children should be identified at an early stage to initiate proper care.
The high CBCL total, internalizing and externalizing scores in the FDD-group show that these children are not only impaired by attentional and hyperac-tive problems, but possibly also by other comorbid behavior problems, which can negatively affect treatment outcome and compliance as well. Screening of children with FDDs should therefore be done using broadband screening ques-tionnaires (such as the CBCL), rather than ADHD-specific quesques-tionnaires alone. In order to better understand the relationship between both disorders and to select adequate treatment methods, future research should focus on whether children with FDD and ADHD would benefit from targeted treatment strategies. In addition, future research could potentially benefit from further investigating the link between FDDs and ADHD, e.g. gastrointestinal motility testing in chil-dren with FDDs with and without ADHD.
CONCLUSION
In this study, 10.3% of children with FDDs had ADHD and 22.7% of children with a known diagnosis of ADHD fulfilled the Rome criteria for a FDD. This suggests that screening for behavioral disorders and defecation disorders should be incorporated into the diagnostic workup of these groups of children. Further research is necessary to further unravel the possible joint pathophysiology of FDDs and ADHD and to assess whether these children would benefit from targeted treatment strategies.
Acknowledgments
The authors would like to thank all clinicians for their help with the inclusion of patients at the outpatient clinic and D.S. van Casteren for her help in collecting the data.
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REFERENCES
1 Hyams JS, Di Lorenzo C, Saps M, et al. Func-tional Disorders: Children and Adolescents. Gastroenterology. 2016.
2 Mugie SM, Benninga MA, Di Lorenzo C. Epide-miology of constipation in children and adults: a systematic review. Best Pract Res Clin Gastro-enterol. 2011;25(1):3–18.
3 Koppen IJN, von Gontard A, Chase J, et al. Management of functional nonretentive fecal incontinence in children: Recommendations from the International Children’s Continence Society. J Pediatr Urol. 2016;12(1):56–64.
4 van Dijk M, Benninga MA, Grootenhuis MA, et al. Chronic childhood constipation: a review of the literature and the introduction of a protocolized behavioral intervention program. Patient Educ Couns. 2007;67(1-2):63–77. 5 van Dijk M, Benninga MA, Grootenhuis MA, et
al. Prevalence and associated clinical charac-teristics of behavior problems in constipated children. Pediatrics. 2010;125(2):e309–17.
6 Benninga MA, Voskuijl WP, Akkerhuis GW, et al. Colonic transit times and behaviour profiles in children with defecation disorders. Arch Dis Child. 2004;89(1):13–6.
7 Ibrahim SH, Voigt RG, Katusic SK, et al. Inci-dence of gastrointestinal symptoms in children with autism: a population-based study. Pediat-rics. 2009;124(2):680–6.
8 McKeown C, Hisle-Gorman E, Eide M, et al. Association of constipation and fecal incon-tinence with attention-deficit/hyperactivity disorder. Pediatrics. 2013;132(5):e1210–5.
9 Peeters B, Noens I, Philips EM, et al. Autism spectrum disorders in children with func-tional defecation disorders. J Pediatr. 2013;163(3):873–8.
10 Diagnostic and statistical manual of mental disorder – Fifth Edition (DSM 5). American Psychiatric Association (APA). Washington, D.C.:American Psychiatric Association 2013. 11 Niemczyk J, Equit M, Hoffmann L, et al.
Inconti-nence in children with treated attention-deficit/
hyperactivity disorder. J Pediatr Urol. 2015; 11(3):141.e1–6.
12 Nøvik TS, Hervas A, Ralston SJ, et al. Influence of gender on attention-deficit/hyperactivity disorder in Europe--ADORE. Eur Child Adolesc Psychiatry. 2006;15 Suppl 1:I15–24.
13 Thapar A, Cooper M. Attention deficit hyper-activity disorder. Lancet. 2016;387(10024): 1240– 1250.
14 Rasquin A, Di Lorenzo C, Forbes D, et al. Childhood functional gastrointestinal disor-ders: child/adolescent. Gastroenterology. 2006;130(5):1527–37.
15 Achenbach T. Manual for the Child Behavior Checklist/4-18 and 1991 Profiles. Burlingtong, VT: Univeristy of Vermont Department of Psychiatry; 1991.
16 Verhulst F, van der Ende J, Koot H. Manual for the Child Behavior Checklist/4-18 and 1991 Profiles [in Dutch]. Rotterdam, Nether-lands; Afdeling Kinder- en JEugdpsychiatrie, Sophia Kinderziekenhuis/Academisch Ziek-enhuis Rotterdam/Erasmus Universiteit van Rotterdam; 1996.
17 Oosterlaan J, Baeyens D, Scheres A, et al. Manual vor behavior problems in children 6-16 years, Manual [In Dutch]. Amsterdam, The Netherlands; 2008.
18 Le HH, Hodgkins P, Postma MJ, et al. Economic impact of childhood/adolescent ADHD in a European setting: the Nether-lands as a reference case. Eur Child Adolesc Psychiatry. 2014;23(7):587–98.
19 Niemczyk J, Equit M, Braun-Bither K, et al. Prevalence of incontinence, attention deficit/ hyperactivity disorder and oppositional defiant disorder in preschool children. Eur Child Adolesc Psychiatry. 2015;24(7):837–43. 20 Joinson C, Heron J, Butler U, et al.
Psycho-logical differences between children with and without soiling problems. Pediatrics. 2006;117(5):1575–84.
LM, et al. Screening for autism identifies behavioral disorders in children functional defecation disorders. Eur J Pediatr. 2016. doi:10.1007/s00431-016-2775-x.
22 Benninga MA, Büller HA, Heymans HS, et al. Is encopresis always the result of constipa-tion? Arch Dis Child. 1994;71(3):186–93. 23 Niemczyk J, Equit M, Hoffmann L, et al.
Incontinence in children with treated atten-tion-deficit/hyperactivity disorder. J Pediatr Urol. 2015;11(3):141.e1–6.
24 Loening-Baucke V. Prevalence rates for constipation and faecal and urinary incon-tinence. Arch Dis Child. 2007;92(6):486–9. 25 Nurko S, Scott SM. Coexistence of
consti-pation and incontinence in children and adults. Best Pract Res Clin Gastroenterol. 2011;25(1):29–41.
26 von Gontard A, Baeyens D, Van Hoecke E, et al. Psychological and psychiatric issues in urinary and fecal incontinence. J Urol. 2011;185(4):1432–6.
27 Loening-Baucke V. Functional fecal reten-tion with encopresis in childhood. J Pediatr Gastroenterol Nutr. 2004;38(1):79–84.
28 Loening-Baucke V. Urinary incontinence and urinary tract infection and their resolution with treatment of chronic constipation of childhood. Pediatrics. 1997;100(2 Pt 1):228–32. 29 von Gontard A, Moritz AM, Thome-Granz
S, et al. Association of attention deficit and elimination disorders at school entry: a popu-lation based study. J Urol. 2011;186(5):2027–32. 30 von Gontard A, Equit M. Comorbidity of ADHD and incontinence in children. Eur Child Adolesc Psychiatry. 2015;24(2):127–40.
31 Duel BP, Steinberg-Epstein R, Hill M, et al. A survey of voiding dysfunction in children with attention deficit-hyperactivity disorder. J Urol. 2003;170(4 Pt 2):1521–3; discussion 1523–4. 32 Burgers R, Liem O, Canon S, et al. Effect of
rectal distention on lower urinary tract func-tion in children. J Urol. 2010;184(4 Suppl):1680– 5.
33 Crimmins CR, Rathbun SR, Husmann DA.
Management of urinary incontinence and nocturnal enuresis in attention-deficit hyper-activity disorder. J Urol. 2003;170(4 Pt 1):1347– 50.
34 Franco I. New ideas in the cause of bladder dysfunction in children. Curr Opin Urol. 2011;21(4):334–8.
35 Shreeram S, He J-P, Kalaydjian A, et al. Prevalence of enuresis and its association with attention-deficit/hyperactivity disorder among U.S. children: results from a nation-ally representative study. J Am Acad Child Adolesc Psychiatry. 2009;48(1):35–41.
36 van Everdingen-Faasen EQ, Gerritsen BJ, Mulder PGH, et al. Psychosocial co-mor-bidity affects treatment outcome in chil-dren with fecal incontinence. Eur J Pediatr. 2008;167(9):985–9.
37 van Dijk M, Bongers MEJ, de Vries G-J, et al. Behavioral therapy for childhood constipa-tion: a randomized, controlled trial. Pediat-rics. 2008;121(5):e1334–41.
